A hierarchical model for external electrical control of an insect, accounting for inter-individual variation of muscle force properties

Elife. 2023 Sep 13:12:e85275. doi: 10.7554/eLife.85275.

Abstract

Cyborg control of insect movement is promising for developing miniature, high-mobility, and efficient biohybrid robots. However, considering the inter-individual variation of the insect neuromuscular apparatus and its neural control is challenging. We propose a hierarchical model including inter-individual variation of muscle properties of three leg muscles involved in propulsion (retractor coxae), joint stiffness (pro- and retractor coxae), and stance-swing transition (protractor coxae and levator trochanteris) in the stick insect Carausius morosus. To estimate mechanical effects induced by external muscle stimulation, the model is based on the systematic evaluation of joint torques as functions of electrical stimulation parameters. A nearly linear relationship between the stimulus burst duration and generated torque was observed. This stimulus-torque characteristic holds for burst durations of up to 500ms, corresponding to the stance and swing phase durations of medium to fast walking stick insects. Hierarchical Bayesian modeling revealed that linearity of the stimulus-torque characteristic was invariant, with individually varying slopes. Individual prediction of joint torques provides significant benefits for precise cyborg control.

Keywords: Carausius morosus; computational biology; external electrical control; hierarchical Bayesian model; inter-individual variation; muscle force property; stick insect; systems biology.

Plain language summary

Hybrid insect-computer robots – an exciting fusion of biology and technology – herald a future of small, highly mobile and efficient devices. However, these robots require a way to control the movements of the insects, a task made complex due to the differences between different insects’ nervous and muscle systems. To bridge this gap, Owaki, Dürr and Schmitz studied the relationship between electrical stimulation of three leg muscles in the legs of stick insects and the resultant torque. To do these experiments, the scientists kept the body of the stick insects fixed and electrically stimulated one out of three leg muscles to produce walking-like movements. The results of these electrical stimulations allowed Owaki, Dürr and Schmitz to propose a model that predicts the torque created in the insect's joints when different patterns of electrical stimulation are applied to a leg muscle. The researchers identified a near-linear relationship between the duration of the electrical stimulus and the resultant torque. Moreover, the slope of this linear relationship can be estimated for individual animals with a few measurements only. This finding refines the precision of the motor control required to build individually tuned biohybrid robots. Investigating the precise control of insect biohybrid robots, particularly using stick insects, can lead to advancements in biohybrid robotics and enrich our understanding of insect locomotion. Owaki, Dürr and Schmitz’s insights could lead to the creation of adaptable and highly mobile devices with many applications, but key challenges need to be addressed. First, model testing must be implemented in free-walking insects, and the electrical stimuli must be refined to mimic natural neuromuscular signals more closely.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bayes Theorem
  • Electric Stimulation
  • Insecta*
  • Movement*
  • Muscles

Associated data

  • Dryad/10.5061/dryad.wpzgmsbsw

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.